Poultry Feathers and Skin: The Poultry Integument in Health and Welfare

By Sunday A. Adedokun, Piter Bijma, Avigdor Cahaner and 14 more

The feathers and skin in birds are the first line of defence, but are also important in helping the bird to maintain a stable internal temperature, facilitate integral mobility and ensure successful mating in some species. For poultry, the physical conditions of feathers and skin are important barometers to assess the impact of management and ensure health and welfare. Based on the proceedings of a recent symposium, this book documents the significant developments that have been made in our understanding of the importance of the integument to poultry species. The book:

. Traces the development of the integument over time and discusses our current understanding of its embryonic development.
. Includes a broad range of studies covering genetics, welfare, health, nutrition, and management.
. Promotes research opportunities in an under-studied field.

Providing a comprehensive yet concise summary of the available research, this book is an invaluable resource for both the poultry industry and for researchers in animal science and welfare at undergraduate and graduate levels.

• Language: English
• Publisher: CAB International
• Release date: Mar 11, 2019
• ISBN: 9781786395122

Book preview

PART I

About the Feather and Its Development

CHAPTER 1

The Feather, a Triumph of Natural Engineering and Multifunctionality

Theagarten Lingham-Soliar*

Nelson Mandela University, South Campus, Port Elizabeth, South Africa

ABSTRACT

Structures in nature have evolved over millions of years and, unlike in engineering, are multifunctional. For example, an airplane wing may perform only a single function: lift. This is unlike the bird wing which, besides also producing power, has an ability to detect local updraught information along the entire surface of the wing such as changes in the distribution of pressure that are vital to soaring and energy saving. This chapter demonstrates how multifunctionality of the feather has enabled vital aspects of bird life. Three of these, involving flight, protection and temperature control, are discussed.

The feather is a structure central to bird flight and the rachis is the central structure of the feather. Syncytial barbule fibres in the rachis are long continuous strands with intermittent hooked nodes, which contribute with the matrix to form the most effective bonding mechanisms known in nature. The unique micro-structure of feathers that has enabled flight has also contributed to a tough outer integument that protects the bird against predators and the environment. Feathers are organized into tracts or pterylae with spaces, the apteria. This system of feather arrangement enables a dense layering of the feathers for mechanical protection without impeding movement. The apteria also help to reduce the total weight of the feathering, which is important for flight.

The precise design of the barbule with nodes and hooks is fundamental to the process of thermoregulation in down feathers. The embryonic down feathers of chicks form individual ‘clumps’ of more or less circular masses that have a tree-like, highly organized self-similar structure, which is crucial to its thermal properties. Each tree-like assemblage comprises a barb and branching barbules, described as primary and secondary structures, attached to the skin by a quill. The whole structure creates a ‘fluffiness’ that helps to trap the warm air.

INTRODUCTION

When vertebrates moved on to land hundreds of millions of years ago, one of the major changes involved a fundamental development of the skin with – for the first time – a distinctive epidermis and the development of a complete body covering of scales. The epidermis was capable of providing mechanical protection, preventing desiccation and providing ultraviolet protection, which together with the dermis provided a double layer of protection. The momentous development was in the composition of the scales of an entirely new material: b-keratin, which is extremely tough and stable and, critically, extremely lightweight. The properties of b-keratin would be applied to the development of the feather and it is probably safe to say that bird flight would not have evolved were it not for this material (Lingham-Soliar, 2014b). Most aspects of bird life are inextricably linked to feather structure and evolution. This chapter looks at the role the feather has played in three vital and fundamental aspects of bird life: flight, protection and thermoregulation.

FEATHERS AND FLIGHT

The arrangement of wing feathers (remiges) and tail feathers (rectrices) is shown for a bird of prey (Fig. 1.1).

The longest wing feathers are the primaries, which extend from the carpal (‘wrist’) joint towards the wing tip (Fig. 1.2). They are generally numbered from the carpal joint to the end of the extended wing (descendent system) (LinghamSoliar, 2015), although in some literature the primary feathers are numbered from the wing tip to the carpal joint (ascendant system).

Fig. 1.1. Location and nomenclature of wing and tail feathers in the Cape vulture, Gyps caprotheres. The left wing shows the internal skeletal structure. Modified from Lingham-Soliar (2015).

The shorter secondary flight feathers grow from the ulna (forewing bone); these are always numbered from the carpal joint inwards towards the body. The innermost secondaries are also referred to as tertials or tertiaries, especially for passerine birds such as the raven (Proctor and Lynch, 1993). The primaries and secondaries together form the lifting surface of the wing.

The typical feather consists of a central shaft (rachis), applied to the portion of the axis of the feather that in life protrudes from the skin, and the lower part, which penetrates the skin and provides attachment and is termed the calamus or quill. Arising from the rachis are serial paired branches (barbs) extending out from the shaft at an angle and lying parallel to each other (Lingham-Soliar, 2017). The barbs possess further branches: the barbules. The barbules of adjacent barbs are attached to one another by hooks. The entire system comprising barbs and barbules forms a vane or web on either side of the rachis, providing the lifting surfaces of the wing and tail feathers. This construction ensures the elasticity of the feather web as well as the capacity of the barbs to re-establish linkage if the continuity of the web is interrupted (Fig. 1.2).

Feathers arise from the integument or skin of birds. The skin is fundamentally adapted to their life as active homeothermic (stable independent body temperature) animals. It is generally thin in areas covered by feathers and thick in bare areas. Its germinative layer is like that in reptiles, but the corneous layer is much thinner in birds than in reptiles (Stettenheim, 2000), where in the latter it aids in protection.

Fig. 1.2. Flight feathers in a juvenile peregrine falcon, Falco peregrinus (primaries 2 and 4 missing). The rachis is visible. Inset 1: diagrammatic view of rachis, barbs and barbules. Note that the sizes of the elements are not to scale. Inset 2: enlarged view showing relative sizes of rachis and barbs. Modified from Lingham-Soliar (2015).

Feathers are constructed of compact b-keratin, the keratin of reptiles and birds (sauropsids), a light rigid material (Fraser and Parry, 2008, 2011). The demands on the feather connected with flight are extraordinary: its qualities are almost paradoxical, having to be exceedingly light (or the bird would never leave the ground) and at the same time exceedingly tough to cope with the stresses of flight in which accelerations may reach extremely high g-forces (Clark, 2009). It is beyond the scope of this review to discuss the aerodynamics of bird flight but the reader may be interested in a review on flight in animals and some of the physics involved (Lingham-Soliar, 2015).

Recent research efforts using the microbes (fungus genus Alternaria) that normally parasitize bird feathers in the wild (Lingham-Soliar et al., 2010) have now made it possible to attempt to answer the question that Gordon (1978) had posed many years ago. The unique assemblage of syncytial barbule fibres (SBFs) in the cortex of the rachis and barbs enabled a microstructure with a high ‘work of fracture’. The model showed (Lingham-Soliar, 2014a) that rather than the traditional brick-and-mortar arrangement considered previously (Lingham-Soliar et al., 2010), the architecture was more comparable with the ‘brick-bridge-mortar’ structure proposed for nacre (Song and Bai, 2001; Katti and Katti, 2006).

We know today that the fundamental structural component of the feather rachis is a system of continuous b-keratin SBFs that extend from the base of the rachis in a proximo-distal direction to its tip. Herein lies a problem if birds are to fly. The rachis may be described as a generalized cone of rapidly diminishing volume (Fig. 1.3).

Thus the volume of the cortex available for SBFs will decrease proximo-distally. Consequently, hundreds of SBFs in the rachidial cortex would theoretically have to be terminated before reaching the rachis tip – creating potentially thousands of inherently fatal crack-like defects. These defects of free ends or notches at numerous points of the cortex along the length of the rachis would locally concentrate the stress at each so- called notch (Lingham-Soliar, 2017). Simple mechanics shows that sudden failure in a material begins at a notch or crack that locally concentrates the stress. This is analogous to the scissor- snip a tailor makes before tearing a piece of fabric. Griffith (1921) showed that, according to thermodynamic principles, the magnitude of the stress concentration at a crack tip is dependent on the crack length, i.e. that the strain energy released in the area around the crack length is available for propagating the crack (similar to the scissor- snip). Given that there are thousands of SBFs in the feather, it is clear that there is a dangerous potential of numerous (hundreds of) self- perpetuating cracks in the feather cortex. The rachis of each feather would fail during the stresses of flight, resulting in a ‘crash- and- burn’ catastrophe. Clearly birds had solved the problem. The subject of the study (Lingham-Soliar, 2017) was: how? Briefly, for the first time we discovered that the SBFs of the barbs arise from well within the rachis, giving a stability hitherto unknown. This has not only solved the problem of the Griffith cracks but once again demonstrates the multifunctionality of bird structure in a unique tissue structure of the rachis that profoundly enhances the combined strength of the rachis and barbs.

Fig. 1.3. Feather rachis as a cone. Diagrammatic view of the rachis as a tapering cone showing potential terminations of SBFs (numbered 1–10, along the edge for illustrative convenience) because of the linear decrease in cortex thickness in the proximo-distal direction. Modified from Lingham-Soliar (2017).

FEATHERS AND PROTECTION

Two aspects of protection will be considered. The first is defence against predation and the second is protection from the environment.

It may be a chicken-and-egg question, i.e. which came first: protection or flight? The author’s own view is that flight was the ultimate honing of a structure, the feather, which was evolving over 150 million years plus, from a basic component akin to the syncytial barbule filaments (Lingham-Soliar et al., 2010). The syncytial barbule filaments were already equipped for a highly important function, thermoregulation (see below), which would later be vital to all aspects of bird life.

Even predatory birds such as hawks that prey on other birds in the air are aware of the ineffectiveness of their sharp talons and beak against the prey’s protective densely feathered coat. Instead the hawk kills by diving and striking the bird in the back with its outstretched feet so as to impart a violent acceleration to the bird as a whole, which has the effect of breaking its neck (Gordon, 1978).

Bird feathers play another role during predation attempts that has evolved as a means of escape: birds often lose feathers because predators are more likely to grab feathers on the rump and the back than on the ventral side of an escaping bird. It is better that a predator (e.g. a cat) ends up with a mouthful of feathers than a mouthful of bird. Møller et al. (2006) predicted that ‘the former feathers would have evolved to be relatively loosely attached as an antipredator strategy in species that frequently die from predation’.

The second part of this section considers how the feather has enabled birds to invade every form of environment on the planet. Many birds fly constantly in and out of trees and hedges and other obstacles, often using such cover as a refuge from their enemies. The unique structure of the feather vanes enables birds to get away with local scrapes and abrasions compared with the membranous wings of other active fliers, past and present.

The flat surface or vane of the pennaceous feather is deceptive and gives the impression of a continuous membrane. It was mentioned above that the barbs and barbules are central to the flight surface or venation of the pennaceous feather structure. Regal (1975) described how the interlocking barbules from adjacent barbs lock parts of the feather into a single tough, flat surface. The barbules of adjacent barbs are able to interlock essentially because those along the distal edge (edge away from the body) of a barb bear tiny hooklets that engage the unhooked (flange-bearing) barbules branching from the proximal edge (edge towards the body) of the adjacent barb. This is seen graphically in a scanning electron microscope (SEM) image of a barb (close to the rachis) in the peregrine falcon, Falco peregrinus (Fig. 1.4).

The system works like opposite pieces of Velcro and is as easily separated and reconnected. Thus, when forces are applied to the surface of this vane, part of the force will be absorbed in elastic deformation of the complex system, or if the force is too great the counterpart barbules will separate and either reattach automatically, or if not, when the bird preens or nibbles its feathers, i.e. runs its beak along the separated barbules to reconnect them to the interlocked state. To put it simply, feathers avoid tears by having a structure that actually enables tearing but with the all- important differences: it occurs as part of a precise design and it is self- repairing or with a little attention from the bird.

Fig. 1.4. Mechanical structure of syncytial barbule cells (fibres). (A) Syncytial barbule cells in the cortex of the feather rachis showing nodes. (B) Detail of the syncytial barbule cells comprising fibrils. (C) Diagrammatic representation of fibre bundling (syncytial barbules) in three dimensions. (D) Diagrammatic brick-bridge-mortar structure between syncytial barbules and polymer matrix demonstrating crack-stopping mechanisms (see text). Scale bar 5 μm. After Lingham-Soliar (2014c), courtesy of Springer, Heidelberg.

This remarkable flight surface of feathers together with the formation into thick layers has enabled birds to live in densely structured habitats where even the loss of a reasonable number of feathers is a small price to pay for their ecological versatility. Besides, birds have one more ‘ace up their sleeve’. When feathers may become too ragged for repair and inefficient, they are simply replaced. Most bird species moult their entire plumage at least once a year and in a few species twice.

THERMOREGULATION

All animals control their body temperature by a process known as thermoregulation, wherein the internal environment of the body is under the influence of both external and internal conditions. There are different ways in which terrestrial animals thermoregulate, such as behaviourally, by moving to a colder or warmer place, by activity to generate body heat, or by panting or sweating to lose it. They also thermoregulate physiologically, by activating internal metabolic processes that warm or cool the blood.

Today’s mammals and birds have a high metabolism and are considered endotherms, which produce body heat internally. They possess biological temperature sensors that control heat production and switch on heat-loss mechanisms such as perspiration. Birds conserve body heat with specially constructed down feathers (Fig. 1.5).

Producing internal heat is one thing but it is an energetically expensive process and has to be conserved. Birds have to conserve their internally produced body heat and they do it uniquely, by growing feathers. Although all feathers are capable of both conserving or dissipating body heat in birds, this section considers the embryonic or down feathers and how they are specialized for insulation (Fig. 1.5).

The shape of down feathers is vital to their performance and primary purpose, which is to provide insulation. Down feathers form individual ‘clumps’ of more or less circular masses (as opposed to the flattened shape of flight feathers) that have a ‘tree-like’, highly organized self-similar structure (Yan and Wang, 2009), which is crucial to their thermal properties (Gao et al., 2009). Each tree-like assemblage comprises a barb and branching barbules, described as primary and secondary structures, attached to the skin by a quill. The microstructure of barbs and barbules have been described in detail (Lingham-Soliar et al., 2010; Lingham-Soliar and Murugan, 2013) and apply equally to the corresponding structures in down feathers.

Hooks (or hooklets) and nodes are vital features of the barbules of down feathers. To the author’s knowledge, only the Silkie’s down feather lacks hooklets (Feng et al., 2014). These tiny hooks keep the barbules from becoming matted and flattened. In this way, the barbs and barbules remain fluffy, trapping air in the plumage for thermal insulation (Stettenheim, 2000). Of great importance too is the stiffness or Young’s modulus of down feathers, especially with respect to the compressive resistance of each tree-like clump, i.e. it should retain its fluffy shape and avoid being compressed or, if compressed, possess enough elasticity to regain its former state. This compressive resistance is closely related to bending resistance and buckling resistance with respect to the microstructural properties of the rachis.

Fig. 1.5. Down feather, Gallus gallus. (A) Down feather showing barb and branching barbules. (B) Detail of the barbules. Some nodes lack (or have reduced) hooks, others have long hooks.

Continued research into the shape of the tree-like clumps, diameter of the barbs and structure of the nodes and hooks of the barbules in different birds is of considerable interest to multi-million-dollar industries involved in the manufacture of bedding and outdoor clothing. One of the problems in the use of downy feathers in the manufacture of outdoor wear is water resistance. Down feathers become ineffective in insulation and thermoregulation when wet or damp. This is immediately obvious in observations of chicks with wet down feathers, which may die rapidly from chill. Perhaps genetic manipulation to produce an ideal down feather will solve some of the problems in commercially utilized down feathers. Certainly more intensive research is called for with respect to down feather microstructure.

REFERENCES

Clark, C.J. (2009) Courtship dives of Anna’s hummingbird offer insights into flight performance limits. Proceedings of the Royal Society London B. doi: 10.1098/rspb.2009.0508

Feng, C., Gao, Y., Dorshorst, B., Song, C., Xiaorong, G. et al. (2014) A cis-regulatory mutation of PDSS2 causes silky-feather in chickens. PLOS Genetics 10(8), e1004576. doi: 10.1371/journal.pgen.1004576

Fraser, R.D.B. and Parry, D.A.D. (2008) Molecular packing in the feather keratin filament . Journal of Structural Biology 162, 1–13. doi: 10.1016/j.jsb.2008.01.011.

Fraser, R.D.B. and Parry, D.A.D. (2011) The structural basis of the filament-matrix texture in the avian/reptilian group of hard b-keratins. Journal of Structural Biology 173, 391–405.

Gao, J., Pan, N. and Yu, W. (2009) Fractal character forecast of down fiber assembly microstructure. Journal of Textile Institute 100(6) 539–544. doi: 10.1080/00405000802055500

Gordon, J.E. (1978) Structures. Penguin, Harmondsworth, UK.

Griffith, A.A. (1921) The phenomena of rupture and flow in solids. Philosophical Transactions of the Royal Society A (London) 221, 163–198.

Katti, K.S and Katti, D.R. (2006) Why is nacre so tough and strong? Material Science Engineering 26, 1317–1324.

Lingham-Soliar, T. (2014a) Feather structure, biomechanics and biomimetics: the incredible lightness of being. Journal of Ornithology 155, 323–336. doi: 10.1007/s10336-013-1038-0.

Lingham-Soliar, T. (2014b) Response to comments by C. Palmer on my paper, Feather structure, biomechanics and biomimetics: the incredible lightness of being. Journal of Ornithology. doi: 10.1007/s10336-014-1093-1

Lingham-Soliar, T. (2014c) The Vertebrate Integument, Volume 1. Springer, Heidelberg, Germany.

Lingham-Soliar, T. (2015) The Vertebrate Integument, Volume 2. Springer, Heidelberg, Germany.

Lingham-Soliar, T. (2017) Microstructural tissue-engineering in the rachis and barbs of bird feathers. Scientific Reports 7, 45162. doi: 10.1038/srep45162.

Lingham-Soliar, T. and Murugan, N. (2013) A new helical crossed-fiber structure of b-keratin in flight feathers and its biomechanical implications. PLOS ONE 8, 1–12.

Lingham-Soliar, T., Bonser, R.H.C. and Wesley-Smith, J. (2010) Selective biodegradation of keratin matrix in feather rachis reveals classic bioengineering. Proceedings of the Royal Society B: Biological Sciences 277(1685), 1161–1168. doi: 10.1098/rspb.2009.1980.

Møller, A.P., Nielsen, J.T. and Erritzøe, J (2006) Losing the last feather: feather loss as an antipredator adaptation in birds. Behavioral Ecology 17, 1046–1056. doi: 10.1093/beheco/arl044

Proctor, N.S. and Lynch P.J. (1993) Manual of Ornithology: Avian Structure and Function. Yale University Press, New Haven, Connecticut.

Regal, P.J. (1975) The evolutionary origin of feathers. The Quarterly Review of Biology 50 (1), 35–66.

Song, F. and Bai, Y. (2001) Analysis of the strengthening and toughening of a biomaterial interface science. China Series. Mathematics 44(12), 1596–1601. doi: 10.1007/BF02880799

Stettenheim, P.R. (2000) The integumentary morphology of modern birds – an overview. American Zoologist 40, 461–477. doi: 10.1093/icb/40.4.461.

Yan, X. and Wang, Y. (2009) A feather and down category recognition system based on GA and SVM. 2009 International Conference on Education Technology and Computer. IEEE Computer Society, Washington. Available at: http://ieeexplore.ieee.org/lpdocs/epic03/wrapper.htm?arnumber=5169466 (accessed 4 October 2018).

*[e-mail]

CHAPTER 2

Embryonic Development of the Avian Integument

Denis Headon*

The Roslin Institute and Royal (Dick) School of Veterinary Studies, University of Edinburgh, UK

ABSTRACT

The skin and its appendages, such as feathers and scales, form the interface between a bird and its environment. The size, number and distribution of feathers and the structure of the skin are defined during embryonic development through interactions between the dermal and epidermal tissues. A number of spontaneous mutations that alter feather distribution in the domestic chicken have been identified, defining key genes and intercellular signals that operate to determine their arrangement. This review summarizes the processes operating and structures formed during embryonic skin development in birds, and the origins of diversity in external appearance that arises from genetic variants acting in this period.

AVIAN SKIN STRUCTURE AND COMPONENTS

The avian skin functions as a barrier to water loss and infection, and in thermo-regulation, display, camouflage and resistance to abrasion. As in other vertebrates, the skin is composed of an epithelium, called the epidermis, attached to a deeper connective tissue, called the dermis. The barrier functions of skin are largely carried out by the epidermis, which is a sheet of cells several layers thick. Most of the cells in the epidermis are keratinocytes, which adhere tightly to one another through cell–cell contacts and produce keratin to form a cytoskeleton. Adherens junctions and desmosomes fasten cells to one another, with the desmosomes connecting keratin cytoskeletons of adjacent cells to make a strong meshwork resistant to mechanical strain (Hatzfeld et al., 2017). The proteins forming these junctions in chicken epidermis function in the same manner as those in the skin of other vertebrates, including mammals, so that avian cells can readily attach to cells from species of different classes if cultured together (Mattey and Garrod, 1985). The cells at the base of the epidermis attach to a basement membrane, a very thin sheet of extracellular material that separates epidermis from dermis. The basal epidermal cells are those that divide, the cells departing the basement membrane stop dividing and instead mature to produce different keratins and lipids that will form the surface barrier. At the surface they lack nuclei and are shed continually and replenished by proliferation below. The epidermis sits atop and attached to the dermis, a connective tissue. This region is characterized by a substantial amount of extracellular material, particularly collagen fibres, and the predominant cells are the fibroblasts, which produce the connective tissue. The dermis carries the skin’s blood vessels, lymphatics, nerves, fat and muscle (Pass, 1995; Stettenheim, 2000). This basic structure of the skin is dramatically altered to produce appendages: the feathers, scales, spurs, glands and the specialized skin of the beak and legs. Generally, in the appendages the epithelial component, derived from the epidermis, is the more active, either proliferating and keratinizing to make the feather or scale, or producing